Burns served as the head baseball coach and assistant football coach with the University of Hawaii in 1951. Burns left Hawaii to coach at Whittier College in 1952, where he was the head basketball coach and an assistant football coach. At the beginning of 1953, he left Whittier and took a job as head football and head basketball coach at St. Mary's of Redford High School in Detroit, Michigan. Following the 1953 football season at St. Mary's, Burns was hired by fellow Michigan alumnus Forest Evashevski as an assistant coach at the University of Iowa. Burns began serving as an assistant coach at Iowa under Evashevski in 1954.
Burns served seven total years as an assistant coach to Evashevski. As part of a deal with Iowa Athletic Board, Evy was appointed as Iowa's athletic director and agreed to appoint his successor as head football coach at Iowa. Evy appointed Burns to succeed him, and Burns became Iowa's 20th head football coach beginning with the 1961 season. He was 34 years old. Before his first game as a college head coach, his 1961 Hawkeye team was named as the preseason number one team in the nation in the AP Poll. Iowa defended their ranking by winning their first four games in 1961, but then the Hawks hit a slide, losing their next four. In their final game of the year, the Hawkeyes defeated Notre Dame, 42–21. It was Iowa's fifth win in six years over the Irish. Iowa finished the season 5–4, their last winning record until 1981. In 1962, for the only time in school history, Iowa defeated both Michigan and Ohio State in the same year. The Hawkeyes won only two other games and posted a 4–5 final record. The school's final game of the season against Notre Dame was canceled on account of the assassination of John F. Kennedy. The Hawkeyes finished 1963 with a 3–3–2 record. A 3–0 start in the 1964 season quickly turned sour, as the Hawkeyes lost their final six games. Burns was now in real danger of being fired, but Iowa had several players returning in 1965, and the Hawkeyes were expected to be very good. Burns was allowed to return in 1965. Before the 1965 season, Playboy Magazine picked Iowa as their preseason number one team in the nation and predicted a 9–1 record for the Hawks. Instead, Iowa finished the year 1–9, and before Iowa's final game that season, it was announced that Burns would not be retained in 1966. Of his firing, Burns said, "I want to be emphatic. I hold no ill feelings toward anyone. I hope, I sincerely hope, Iowa has great success in football in the future. If I can contribute to that future, I will." After his final game, his players hoisted him on their shoulders and carried him off the field, despite the loss. There were those who insisted that Forest Evashevski wanted to be called back as football coach and that rather than helping Burns to succeed, Evy hampered him with rules and regulations that were not in force when Evy was the coach. But Burns ultimately said, "If we have failed, and we have, I'll take the responsibility for that. It is not the players' fault. They have done the best they can." He had a 16–27–2 record at Iowa.
Professional coaching career
Burns was 38 years of age when he was fired at Iowa. He moved on to the Green Bay Packers of the NFL and served for two years as an assistant coach to Vince Lombardi in 1966 and 1967 when the Packers won Super Bowl I and Super Bowl II. When Lombardi retired after the 1967 season, Burns was hired by Bud Grant of the Minnesota Vikings. Grant hired Burns to be his offensive coordinator. Burns served as Minnesota's offensive coordinator for the next 18 years, from 1968–1985. During that time, the Vikings made the playoffs 12 times, won 11 division titles, and played in four Super Bowls. When Grant retired from coaching for the second time in 1985, Burns was named as the 4th head coach of the Minnesota Vikings on January 7, 1986. He coached Minnesota for six years, from 1986 to 1991. Burns compiled a record of 52–43 and led the Vikings to the playoffs three times. He helped the Vikings win the division title in 1989 and led them to the NFC championship game in 1987. On November 5, 1989, Burns gave a profanity laced tirade during a postgame press conference where he defended his offensive coordinator, Bob Schnelker, despite the fact that the Vikings' Rich Karlis kicked a then league record-tying seven field goals en route to a 23-21 overtime victory over the Los Angeles Rams. On December 4, 1991, Burns announced that he would retire from coaching after the 1991 NFL season; he finished his final season with an 8-8 record. He has been nominated for the Pro Football Hall of Fame, but has yet to gain the votes necessary for induction. In 1998, Burns gave the Hall of Fame induction speech for Paul Krause, a defensive back he coached both at Iowa and with the Vikings.